Literature DB >> 28615330

The visual encoding of purely proprioceptive intermanual tasks is due to the need of transforming joint signals, not to their interhemispheric transfer.

Léo Arnoux1, Sebastien Fromentin1, Dario Farotto1, Mathieu Beraneck1, Joseph McIntyre1,2,3, Michele Tagliabue4.   

Abstract

To perform goal-oriented hand movement, humans combine multiple sensory signals (e.g., vision and proprioception) that can be encoded in various reference frames (body centered and/or exo-centered). In a previous study (Tagliabue M, McIntyre J. PLoS One 8: e68438, 2013), we showed that, when aligning a hand to a remembered target orientation, the brain encodes both target and response in visual space when the target is sensed by one hand and the response is performed by the other, even though both are sensed only through proprioception. Here we ask whether such visual encoding is due 1) to the necessity of transferring sensory information across the brain hemispheres, or 2) to the necessity, due to the arms' anatomical mirror symmetry, of transforming the joint signals of one limb into the reference frame of the other. To answer this question, we asked subjects to perform purely proprioceptive tasks in different conditions: Intra, the same arm sensing the target and performing the movement; Inter/Parallel, one arm sensing the target and the other reproducing its orientation; and Inter/Mirror, one arm sensing the target and the other mirroring its orientation. Performance was very similar between Intra and Inter/Mirror (conditions not requiring joint-signal transformations), while both differed from Inter/Parallel. Manipulation of the visual scene in a virtual reality paradigm showed visual encoding of proprioceptive information only in the latter condition. These results suggest that the visual encoding of purely proprioceptive tasks is not due to interhemispheric transfer of the proprioceptive information per se, but to the necessity of transforming joint signals between mirror-symmetric limbs.NEW & NOTEWORTHY Why does the brain encode goal-oriented, intermanual tasks in a visual space, even in the absence of visual feedback about the target and the hand? We show that the visual encoding is not due to the transfer of proprioceptive signals between brain hemispheres per se, but to the need, due to the mirror symmetry of the two limbs, of transforming joint angle signals of one arm in different joint signals of the other.
Copyright © 2017 the American Physiological Society.

Entities:  

Keywords:  bimanual movements; goal-oriented hand movements; kinesthesia; sensory encoding; sensory transformations

Mesh:

Year:  2017        PMID: 28615330      PMCID: PMC5596132          DOI: 10.1152/jn.00140.2017

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  51 in total

1.  Bayesian integration in sensorimotor learning.

Authors:  Konrad P Körding; Daniel M Wolpert
Journal:  Nature       Date:  2004-01-15       Impact factor: 49.962

2.  Proprioceptive acuity assessment via joint position matching: from basic science to general practice.

Authors:  Daniel J Goble
Journal:  Phys Ther       Date:  2010-06-03

3.  The effects of landmarks on the performance of delayed and real-time pointing movements.

Authors:  Sukhvinder S Obhi; Melvyn A Goodale
Journal:  Exp Brain Res       Date:  2005-07-22       Impact factor: 1.972

4.  The effect of target modality on visual and proprioceptive contributions to the control of movement distance.

Authors:  Fabrice R Sarlegna; Robert L Sainburg
Journal:  Exp Brain Res       Date:  2007-01       Impact factor: 1.972

5.  Egocentric and allocentric constraints in the expression of patterns of interlimb coordination.

Authors:  S P Swinnen; K Jardin; R Meulenbroek; N Dounskaia; M H Den Brandt
Journal:  J Cogn Neurosci       Date:  1997-05       Impact factor: 3.225

6.  Exploring interlimb constraints during bimanual graphic performance: effects of muscle grouping and direction.

Authors:  S P Swinnen; K Jardin; S Verschueren; R Meulenbroek; L Franz; N Dounskaia; C B Walter
Journal:  Behav Brain Res       Date:  1998-01       Impact factor: 3.332

7.  Role of the supplementary motor area and the right premotor cortex in the coordination of bimanual finger movements.

Authors:  N Sadato; Y Yonekura; A Waki; H Yamada; Y Ishii
Journal:  J Neurosci       Date:  1997-12-15       Impact factor: 6.167

8.  Neural correlates of reliability-based cue weighting during multisensory integration.

Authors:  Christopher R Fetsch; Alexandre Pouget; Gregory C DeAngelis; Dora E Angelaki
Journal:  Nat Neurosci       Date:  2011-11-20       Impact factor: 24.884

9.  Proprioceptive bimanual test in intrinsic and extrinsic coordinates.

Authors:  Riccardo Iandolo; Valentina Squeri; Dalia De Santis; Psiche Giannoni; Pietro Morasso; Maura Casadio
Journal:  Front Hum Neurosci       Date:  2015-02-18       Impact factor: 3.169

10.  Vision of the active limb impairs bimanual motor tracking in young and older adults.

Authors:  Matthieu P Boisgontier; Florian Van Halewyck; Sharissa H A Corporaal; Lina Willacker; Veerle Van Den Bergh; Iseult A M Beets; Oron Levin; Stephan P Swinnen
Journal:  Front Aging Neurosci       Date:  2014-11-17       Impact factor: 5.750

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  2 in total

1.  Neural correlates of lower limbs proprioception: An fMRI study of foot position matching.

Authors:  Riccardo Iandolo; Alessandro Bellini; Catarina Saiote; Ilaria Marre; Giulia Bommarito; Niels Oesingmann; Lazar Fleysher; Giovanni Luigi Mancardi; Maura Casadio; Matilde Inglese
Journal:  Hum Brain Mapp       Date:  2018-01-22       Impact factor: 5.038

2.  How Tilting the Head Interferes With Eye-Hand Coordination: The Role of Gravity in Visuo-Proprioceptive, Cross-Modal Sensory Transformations.

Authors:  Jules Bernard-Espina; Daniele Dal Canto; Mathieu Beraneck; Joseph McIntyre; Michele Tagliabue
Journal:  Front Integr Neurosci       Date:  2022-03-10
  2 in total

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